Neuroscience Letters, 21 (1981) 105-110 105 (~, Elsevier/North-Holland Scientific Publishers Ltd.

S I N G L E U N I T A C T I V I T Y IN M O N K E Y C A U D A T E N U C L E U S D U R I N G

OPERANT BAR PRESSING FEEDING BEHAVIOR

HITOO NISHINO, TAKETOSHI ONO*, MASAJ1 FUKUDA, KAZUO SASAKI and KEN-ICHIRO MURAMOTO

Department of Physiology, Faculty of Medicine, Toyama Medical and Pharmaceutical University, Toyama, 930-01 (Japan)

(Received December 25th, 1979; Revised version received August 14th, 1980; Accepted August 23rd, 1980)

Unit activity and changes during bar press feeding behavior after presentation of food or non-food were analyzed in 198 neurons in the head of the caudate nucleus of monkey. Eight neurons responded uniquely at the sight of food. The degree of the food-specific responses differed depending on the nature of the food and the hunger-satiation state. On the other hand, 17 neurons responded more or less to the sight of food and during bar pressing for food. These two types of neuron seem to be important to bar pressing feeding behavior, which consists of recognition of food and a bar press task to obtain food.

The cauda te nucleus (CD), a m a j o r e x t r a p y r a m i d a l system center , has long been

cons idered to be involved in regula t ing pos ture , muscle tonus , reflex or m o v e m e n t

[3, 8]. C D lesions cause H u n t i n g t o n ' s chorea- l ike s y m p t o m s , and damage in the

dopamine rg i c p a t h w a y which pro jec t s to the neos t r i a tum f rom the m i d b r a i n causes

P a r k i n s o n ' s disease.

In add i t i on , o ther CD funct ions have recent ly been re -eva lua ted because o f the

mass ive , in t ima te in te rconnec t ions with the f ron ta l cor tex [4, 9]. Bi la tera l lesion of

the head o f the CD impa i r ed de layed a l t e rna t ion or de layed response [1, 14].

Decrease o f acquis i t ion ra te , or f lexibi l i ty in a new task , fo l lowed lesion o f the CD

[7, 10]. Some neurons in the head o f the C D changed fir ing ra te in response to

visual , acoust ic or soma tosenso ry s t imula t ion [15], and at the sight o f s ignif icant

s t imuli such as food [2, 5, 13]. Sensory inputs o f mul t imoda l i t i e s are cons idered to

be processed in par t in the cen t romed ian -neos t r i a t a l system [6]. It thus appea r s that

the CD, which s tands be tween the cor t ica l man t l e and mul t i synap t i c efferent pa th ,

may be involved in senso r imoto r in tegra t ion or cogni t ive funct ion [11].

Ope ran t ba r pressing feeding behav io r r epo r t ed in a previous paper [12] was

shown to be accompl i shed by t h o r o u g h in tegra t ion o f the sensory and m o t o r

systems. In the present r epor t we recorded single unit ac t iv i ty in the head o f the

CD dur ing such ope ran t ba r pressing feeding behav io r in o rde r to make clear how

much CD neurons were concerned in: (i) d i sc r imina t ion o f an ob jec t ( food or non-

food) , and (ii) o r i en ta t ion behav ior (bar press ing pe r fo rmance ) which begins a f te r

* To whom all correspondence should be addressed.

106

the recognition of a significant object.

Two Macaca irus (body weights 3.5 and 4.5 kg) were used. The experimental procedure was almost the same as that described previously [12]. Bar press feeding behavior was divided into 3 stages: (1) a discrimination-related stage which started

when an opaque shutter (WI) was opened and the animal could see an object (food or non-food) through a second, transparent shutter (W2); (2) a bar pressing, drive- related stage in which a bar was required to be pressed according to a preset fixed

ratio (FR) schedule to obtain the food; and (3) an ingestion or reward-related stage

which started when W2 was opened by the last bar press, and the monkey took and

ate the food. Unit activity in the head of the CD (A: 21-18, L: 2-6 , H: 10-15) was recorded

with tungsten microelectrodes, and its relation to bar press feeding behavior was analyzed. Signals were fed to a preamplifier, analyzed on line by a minicomputer

(ATAC-450, Nihon Koden Co.), monitored on oscilloscopes and stored in magnetic

tapes. Firing rates per 10 or 100 msec bin, for 64 or 128 points over 0.64, 1.28, 6.4 or 12.8 sec were added for 3-5 trials, and the histograms of firing before and after the

animal saw an object were plotted. Out of 198 neurons recorded in the head of the CD, 41 responded (24 increased,

17 decreased) in the discrimination-related stage when Wj was opened and the animal saw food (initial response). To eliminate the pure sensory responses to the

sound or movement of the window opening, WI was opened with no noise and at different speeds. Ten out of 41 initial responses disappeared in these conditions. The

remaining 31 responses which persisted in all Wj opening conditions were thus regarded as object dependent. The latency of the initial response was between 60 and 300 msec. The shortest latency was observed when neurons responded to pure

sensory factors such as sound or movement when W1 opened, while latency of the responses at the sight of food was somewhat longer (150-300 msec). Thirty-one

neurons which responded at the sight of food were also tested with non-food (screw, pencil or syringe). Eight neurons responded selectively to food and not to non-food

while the remaining 23 responded to both food and non-food in the same manner. Fig. 1 shows typical food-specific responses. Firing increased by different

amounts at the sight of different foods (Fig. IA). The biggest responses occurred when the monkey saw a bean or an orange. Responses at the sight of bread or a cookie were medium, and there was no significant response at the sight of non-food

(screw). The bigger the initial responses, the shorter the latency of the bar press to obtain food (bean, 0.9 sec; orange, 1 sec; bread, 1.1 sec and cookie 1.2 sec). These data might suggest that initial responses could reflect activity which is related to the

initiation of bar press movement. This explanation, however, does not seem to answer the questions of why the firing frequency did not change in association with spontaneous arm movement, and why the initial response still existed even if there was no bar press movement. An example of one of these conditions is shown in Fig.

1B: delayed bar press (BP). Even when the bar was covered for as long as 3 sec and the monkey did not press it, firing increase (initial response) was still observed until

the cover was removed. On the other hand, the initial responses to the bean and cookie were quite

107

CD A

Bean Orange Bread Cookie Screw

11.41 . . . . . . l , . h . . _ i l h , , , - 1 4 h , . .

B Orange Orange Bean delayed BP after satiated after satiated

with Orange with Orange

2 sec

2 s e c

Fig. 1. Responses of CD neurons to different foods and non-food. A and B, upper: histograms of firing; middle: cumulated firing; bottom: bar press signs. Each histogram shows the totaled responses of three trials. Open triangles, time when first shutter (W 0 was opened; dotted lines, extension of pre-trial control firing rate. Scales for histogram of firing and cumulated firing are shown on the right: abscissae, time in sec. A: firing increased (initial response) at sight of food depending upon its nature. The larger the initial response, the shorter the latency to start of bar press. B: the initial response was prolonged when the bar was covered and the monkey could not press the bar even if he wanted to (delayed BP). Response for oranges almost disappeared after the monkey was satiated on oranges but response for beans remained (but weaker) after satiation on oranges.

different from each other although their shapes, sizes and colors were almost the same. In this sense the initial response does not seem to reflect simple sensory input, which depends only on perception of simple physical factors of an object such as color or size, but may indicate an integrated sensory response. Furthermore, the response to an orange almost disappeared after satiation with oranges. On the other hand, the response to a bean still appeared after satiation with oranges, although it was weaker in comparison to the initial response (Fig. 1B). These data suggest that the initial response at the sight of an object reflects not just a simple sensory or a pure motor response but, rather, some integrated motivation which may be coupled with sensorimotor integration.

In the bar pressing, drive-related stage to obtain food, 27 neurons responded (17 increased, 10 decreased). Since the initial response, when it was strong and long- lasting, overlapped into the bar pressing period, a high FR schedule which required 10 bar presses was used to obtain more bar press information free of interference from the initial response. In these situations the initial and following (bar pressing,

1 ()~

drive-related) responses could be separated rather well, and it was found that 17 neurons responded during the bar press stage.

Fig. 2 (upper, raw unit records; lower, histograms of firing) shows examples of

responses at the sight of raisins and during bat pressing. In the FR 3 trial (upper, top), firing increased at the sight of a raisin with 150 msec latency. This excitation

decreased a little but still continued during the bar pressing period. In the first trial at FR 10 (upper, second), the initial response at the sight of a raisin was almost the

same as that observed in the FR 3 trial, and firing increased throughout the bar press task, but the firing response was not so regular. In the 4th trial of FR 10 (upper,

third), however, when the monkey learned that W2 would not open until the 10th bar press, firing remained at a high level and was fairly constant throughout the bar

pressing period. Histograms of three FR 3 trials, FR 10 trials 1-3, and FR 10 trials

4 -6 are shown at the bottom of Fig. 2. In this neuron no significant response was observed at the sight of non-food. Firing responses were not correlated with individual bar press movements. The responses which continue throughout the bar

pressing period are apparently not pure motor coupled responses, but might reflect some internal drive related state to perform bar press activity to obtain food.

C D Raisin

F R 3

F R I O

I

4 ; ! I O O p V

• " " " " * • " " " • | s o c "

F R 3

5 ,,

F R 10

1 - 3

14

mJm, ,

Fig. 2. Response to sight of foods and during bar pressing task in different FR schedules. Upper three

records: raw unit discharges. Open triangles, time when WI was opened; filled triangles, each bar press; filled circles, time when food was put into mouth . Initial response at sight of raisin started 150 msec after

Wl was opened, and continued daring bar pressing period. In first trial at FR l0 (second line), initial response was almost the same as in FR 3 (top), and firing continued during task, but weak and fluctuating. In 4th FR l0 trial (third line), firing during bar press task remained at a high level and fairly

constant. Histograms below show totaled responses o f three trials. Left, FR 3; middle, FR 10 trials 1-3; right, FR l0 trials 4 -6 . Signs on time scales indicate cumulated bar press. Ordinates, ~tV and firing rate

respectively; abscissae, time in sec.

109

Unit response to body movement, or in the ingestion, reward-stage is still under investigation.

In conclusion, this monkey bar press feeding study revealed neurons which respond at the sight of food and throughout the bar press task. These CD neurons seem to have some significance in bar pressing feeding behavior which occurs as a result of integration of the sensory and motor systems.

The authors thank Prof. A. Simpson, Showa University, for help in manuscript preparation, and Mrs. H. Matsuyama for assistance with illustrations. This work was supported in part by the Japanese Ministry of Education, Science and Culture Grant-in-Aid for Special Project Research, 411806, and for Scientific Research, 548098.

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